Skip to main content
SpringerLink
Log in

Organization of Iroquois genes in fish

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

In mammals, a total of six iroquois (Irx) genes exist, which are organized into two clusters. Here we report on the organization of all iroquois genes present in fish, using zebrafish (Danio rerio) and pufferfish (Fugu rubripes and Tetraodon nigroviridis) as examples. A total of 10 Irx genes were found in pufferfish, and 11 in zebrafish; all but one of these genes are organized into clusters (four clusters plus one isolated gene locus). The “extra” fish clusters result from chromosome duplication in the fish lineage, after its divergence from tetrapod vertebrates. Two of the four fish clusters are highly conserved to the ones in mammals, with regard to similarity of genes and cluster architecture. Irx genes within the other two clusters have diverged in sequence and cluster organization, suggesting functional divergence. These results will allow us to use the zebrafish system for functional and comparative studies of iroquois genes in vertebrate development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1 a
Fig. 2
Fig. 3a–f

Similar content being viewed by others

References

  • Amores A, Force A, Yan Y-L, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang Y-L, Westerfield M, Ekker M, Postlethwait JH (1998) Zebrafish hox clusters and vertebrate genome evolution. Science 282:1711–1714

    CAS  PubMed  Google Scholar 

  • Aparicio S (2000) Vertebrate evolution: recent perspectives from fish. Trends Genet 16:54–56

    Article  CAS  PubMed  Google Scholar 

  • Briscoe J, Pierani A, Jessel TM, Ericson J (2000) A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101:435–445

    CAS  PubMed  Google Scholar 

  • Carroll RL (1988) Vertebrate paleontology and evolution. Freeman, New York

  • Cavodeassi F, Modolell J, Gómez-Skarmeta JL (2001) The Iroquois family of genes: from body building to neural patterning. Development 128:2847–2855

    CAS  PubMed  Google Scholar 

  • Cheng CW, Hui C, Strahle U, Cheng SH (2001) Identification and expression of zebrafish Iroquois homeobox gene irx1. Dev Genes Evol 21:442–444

    Article  Google Scholar 

  • Feijóo CG, Manzanares M, de la Calle-Mustienes E, Gómez-Skarmeta JL, Allende ML (2004) The Irx gene family in zebrafish: genomic structure, evolution and initial characterization of irx5b. Dev Genes Evol. DOI 10.1007/s00427-004-0401-9

    Google Scholar 

  • Felsenstein J (1989) PHYLIP—phylogeny inference package (version 3.2). Cladistics 5:164–166

    Google Scholar 

  • Gómez-Skarmeta JL, Modolell J (2002) Iroquois genes: genomic organization and function in vertebrate neural development. Curr Opin Genet Dev 12:403–408

    Google Scholar 

  • Gómez-Skarmeta JL, Diez del Corral R, de la Calle-Mustienes E, Ferrés-Marcó D, Modolell J (1996) Araucan and caupolican, two members of the novel Iroquois complex, encode homeoproteins that control proneural and vein forming genes. Cell 85:95–105

    PubMed  Google Scholar 

  • Gómez-Skarmeta JL, Glavic A, de la Calle-Mustienes E, Modolell J, Mayor R (1998) Xiro, a Xenopus homolog of the Drosophila Iroquois complex genes, controls development at the neural plate. EMBO J 17:181–190

    Article  PubMed  Google Scholar 

  • Gómez-Skarmeta JL, de la Calle-Mustienes E, Modolell J (2001) The Wnt-activated Xiro1 gene encodes a repressor that is essential for neural development and downregulates Bmp4. Development 128:551–560

    PubMed  Google Scholar 

  • Heasman J (2002) Morpholino oligos: making sense of antisense? Dev Biol 15:209–214

    Article  Google Scholar 

  • Houweling AC, Dildrop R, Peters T, Mummenhoff J, Moorman AFM, Rüther U, Christoffels VM (2001) Gene and cluster-specific expression of the Iroquois family members during mouse development. Mech Dev 107:169–174

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi D, Kobayashi M, Matsumoto K, Ogura T, Nakafuku M, Shimamura K (2002) Early subdivisions in the neural plate define distinct competence for inductive signals. Development 129:83–93

    CAS  PubMed  Google Scholar 

  • Kudoh T, Dawid IB (2001) Role of the iroquois3 homeobox gene in organizer formation. Proc Natl Acad Sci USA 98:7852–7857

    Article  CAS  PubMed  Google Scholar 

  • Lecaudey V, Thisse C, Thisse B, Schneider-Maunoury S (2001) Sequence and expression pattern of ziro7, a novel, divergent zebrafish iroquois homeobox gene. Mech Dev 109:383–388

    Article  CAS  PubMed  Google Scholar 

  • Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155

    Article  CAS  PubMed  Google Scholar 

  • McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68:283–302

    CAS  PubMed  Google Scholar 

  • Meyer A, Schartl M (1999) Gene and genome duplications in vertebrates: the one-to-four (to-eight in fish) rule and the evolution of novel gene functions. Curr Opin Cell Biol 11:699–704

    Google Scholar 

  • Mizuguchi R, Sugimori M, Takebayashi H, Kosako H, Nagao M, Yoshida S, Nabeshima Y, Shimamura K, Nakafuku M (2001) Combinatorial roles of Olig2 and Neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motor neurons. Neuron 31:757–771

    Article  CAS  PubMed  Google Scholar 

  • Netter S, Fauvarque MO, Diez del Corral R, Dura JM, Coen D (1998) white + transgene insertions presenting a dorsal/ventral pattern define a single cluster of homeobox genes that is silenced by the Polycomb-group proteins in Drosophila melanogaster. Genetics 149:257–275

    CAS  PubMed  Google Scholar 

  • Novitch BG, Chen AI, Jessell TM (2001) Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31:773–789

    Article  CAS  PubMed  Google Scholar 

  • Ogura K, Matsumoto K, Kuroiwa A, Isobe T, Otoguro T, Jurecic V, Baldini A, Matsuda Y, Ogura T (2001) Cloning and chromosome mapping of human and chicken Iroquois (IRX) genes. Cytogenet Cell Genet 92:320–325

    Article  CAS  PubMed  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer, Heidelberg Berlin New York

  • Peters T, Dildrop R, Ausmeier K, Rüther U (2000) Organization of mouse iroquois homeobox genes in two clusters suggests a conserved regulation and function in vertebrate development. Genome Res 10:1453–1462

    Article  CAS  PubMed  Google Scholar 

  • Postlethwait JH, Yan YL, Gates MA, Horne S, Amores A, Brownlie A, Donovan A, Egan ES, Force A, Gong Z, Goutel C, Fritz A, Kelsh R, Knapik E, Liao E, Paw B, Ransom D, Singer A, Thomson M, Abduljabbar TS, Yelick P, Beier D, Joly JS, Larhammar D, Rosa F, Westerfeld M, Zon LI, Johnson SL, Talbot WS (1998) Vertebrate genome evolution and the zebrafish gene map. Nat Genet 18:345–349

    CAS  PubMed  Google Scholar 

  • Prince VE (2002) The Hox paradox: more complex(es) than imagined. Dev Biol 249:1–15

    Article  CAS  PubMed  Google Scholar 

  • Taylor JS, Van de Peer Y, Braasch I, Meyer A (2001) Comparative genomics provides evidence for an ancient genome duplication event in fish. Philos Trans R Soc Lond B Biol Sci 356:1661–1679

    CAS  PubMed  Google Scholar 

  • Wang X, Emelyanov A, Speptsova-Friedrich I, Korzh V, Gong Z (2001) Expression of two novel zebrafish iroquois homologues (ziro1 and ziro5) during early development of axial structures and central nervous system. Mech Dev 105:191–195

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to acknowledge the critical reading of the manuscript by Thomas Theil and Jeanette Vierkotten. This work has been supported by a grant of the Deutsche Forschungsgemeinschaft through SFB 590.

Author information

Authors and Affiliations

  1. Institute for Animal Developmental and Molecular Biology, University of Düsseldorf, Universitätsstrasse 1, 40225, Düsseldorf, Germany

    Renate Dildrop & Ulrich Rüther

Authors
  1. Renate Dildrop
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ulrich Rüther
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ulrich Rüther.

Additional information

Edited by D. Tautz

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dildrop, R., Rüther, U. Organization of Iroquois genes in fish. Dev Genes Evol 214, 267–276 (2004). https://doi.org/10.1007/s00427-004-0402-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-004-0402-8

Keywords

Search

Navigation